Nucleoli in embryos: a central structural platform for embryonic chromatin remodeling?

Fulka, Helena; Langerova, Alena

doi:10.1007/s10577-018-9590-3

Cited by 14 publications

(8 citation statements)

References 78 publications

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“…For example, structural changes in the nucleolus are often observed in cancer ( Hein et al., 2013 ). Furthermore, the structure and composition of the nucleolus are remarkably different between somatic cells and germ cells and during early development (reviewed in Fulka and Langerova, 2019 ; Kresoja-Rakic and Santoro, 2019 ). As discussed later, these structural changes mirror ribosome biogenesis activities as well as the transcriptional and chromatin states of rRNA genes, and might have implications in genome organization.…”

Section: Main Textmentioning

confidence: 99%

Regulation and Roles of the Nucleolus in Embryonic Stem Cells: From Ribosome Biogenesis to Genome Organization

Gupta

Santoro

2020

Stem Cell Reports

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The nucleolus is the largest compartment of the eukaryotic cell's nucleus. It acts as a ribosome factory, thereby sustaining the translation machinery. The nucleolus is also the subnuclear compartment with the highest transcriptional activity in the cell, where hundreds of ribosomal RNA (rRNA) genes transcribe the overwhelming majority of RNAs. The structure and composition of the nucleolus change according to the developmental state. For instance, in embryonic stem cells (ESCs), rRNA genes display a hyperactive transcriptional state and open chromatin structure compared with differentiated cells. Increasing evidence indicates that the role of the nucleolus and rRNA genes might go beyond the control of ribosome biogenesis. One such role is linked to the genome architecture, since repressive domains are often located close to the nucleolus. This review highlights recent findings describing how the nucleolus is regulated in ESCs and its role in regulating ribosome biogenesis and genome organization for the maintenance of stem cell identity.

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Section: Main Textmentioning

confidence: 99%

Regulation and Roles of the Nucleolus in Embryonic Stem Cells: From Ribosome Biogenesis to Genome Organization

Gupta

Santoro

2020

Stem Cell Reports

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“…When oocytes reach their full size, they acquire the competence to disassemble their nuclei and undergo meiotic maturation. However, not all oocytes have a full developmental potential when fertilized [34]. During the very final growth phase, oocytes acquire two main types of nuclear organization: the surrounded nucleolus (SN) type and the nonsurrounded nucleolus (NSN) type.…”

Section: Nucleolus Structures and Rrna Genes In Gametogenesismentioning

confidence: 99%

Nucleolus and rRNA Gene Chromatin in Early Embryo Development

Kresoja‐Rakic

Santoro

2019

Trends in Genetics

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The nucleolus is the largest substructure in the nucleus and forms around the nucleolar organizer regions (NORs), which comprise hundreds of rRNA genes. Recent evidence highlights further functions of the nucleolus that go beyond ribosome biogenesis. Data indicate that the nucleolus acts as a compartment for the location and regulation of repressive genomic domains and, together with the nuclear lamina, represents the hub for the organization of the inactive heterochromatin. In this review, we discuss recent findings that have revealed how nucleolar structure and rRNA gene chromatin states are regulated during early mammalian development and their contribution to the higher-order spatial organization of the genome. The Multifunctional Nucleolus: From Ribosome Producer to Organizer of Genome Architecture The nucleolus (see Glossary) is the largest subnuclear compartment of the cell and forms around regions of chromosomes containing stretches of tandem repetitive rRNA genes, known as nucleolar organizer regions (NORs). The nucleolus is responsible for the production of ribosomes, a highly regulated process that is essential for growth and development. Ribosome biogenesis is initiated in the nucleolus by RNA polymerase I (Pol I), which, together with a dedicated set of basal transcription factors, such as TIF1A, the TBP-TAFI complex SL1, and the DNA architectural upstream binding factor (UBF) [1,2], transcribes hundreds of rRNA genes to generate 45S/47S pre-rRNA in mammalian cells (Figure 1A). This rRNA precursor is chemically modified and processed to form 28S, 18S, and 5.8S rRNAs, which are then assembled with ribosomal proteins and 5S rRNA and exported from the nucleus to give rise to active ribosomes in the cytoplasm [3]. Increasing evidence suggests that the function of the nucleolus and rRNA genes goes beyond ribosome biogenesis. One aspect that has received significant interest over the past decade is the link between the nucleolus and rRNA genes with the organization of genome architecture. Clustering of heterochromatin at nucleoli is a phenomenon that occurs in all cells. Furthermore, regions located close to the nucleolus (nucleolar-associated domains, NADs) have low gene densities, low transcriptional levels, and repressive histone modifications [4-8]. Since similar heterochromatic and repressive regions are also located to the nuclear lamina, the nucleolus, together with the nuclear lamina, can be considered the hub for the organization of the inactive chromatin in the cell [8-10]. In this review, we address the role of the nucleolus as a subnuclear compartment for the organization of heterochromatin. We discuss recent findings that have revealed how nucleolar structure and rRNA gene chromatin states are regulated during gametogenesis and early mammalian development, and their contribution in the higher-order spatial organization of the genome. Nucleolus and rRNA Genes in Somatic Cells In somatic cells, the nucleolus is a membraneless compartment with a peculiar tripartite architecture: the fibrillar cen...

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“…During the embryonic ZGA period, rRNA synthesis restarts, and the NPBs gradually switch to transcriptionally active nucleoli. 21 Formation of functional nucleoli is accompanied by the activation of ribosomal RNA genes and de novo ribosomal synthesis as major transcriptional activities [28][29][30] occurring at different developmental embryonic stages depending on the mammalian species (e.g., at the 2-cell stage in mice, the 4-cell stage in pigs, and at the 8-cell to 16-cell stages in humans and cows). [31][32][33] In SCNT embryos, the fully differentiated nucleoli disassemble rapidly and then reassemble and form nucleolus-like bodies similar to zygotic pronuclei.…”

Section: Discussionmentioning

confidence: 99%

C23 gene regulates the nucleolin structure and biosynthesis of ribosomes in bovine intraspecific and interspecific somatic cell nuclear transfer embryos

Wang

Gao

et al. 2021

The FASEB Journal

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Somatic cell nuclear transfer (SCNT) can reprogram differentiated somatic cells to produce individual animals, thus having advantages in animal breeding and chromatin reprogramming. Interspecies SCNT (iSCNT) provides extreme cases of reprogramming failure that can be used to understand the basic biological mechanism of genome reprogramming. It is important to understand the possible mechanisms for the failure of zygotic genome activation (ZGA) in iSCNT embryos in order to improve the efficiency of SCNT embryos. In the present study, we compared the development of bovine-bovine (B-B), ovine-ovine (O-O) SCNT, and ovine-bovine (O-B) iSCNT embryos and found that a developmental block existed in the 8-cell stage in O-B iSCNT embryos. RNA sequencing and q-PCR analysis revealed that the large ribosomal subunit genes (RPL) or the small ribosomal subunit genes (RPS) were expressed at lower levels in the O-B iSCNT embryos. The nucleolin (C23) gene that regulates the ribosomal subunit generation was transcribed at a lower level during embryonic development in O-B iSCNT embryos. In addition, the nucleolin exhibited a clear circular-ring structure in B-B 8-cell stage embryos, whereas this was shell-like or dot-like in the O-B embryos. Furthermore, overexpression of C23 could increase the blastocyst rate of both SCNT and iSCNT embryos and partly rectify the ring-like nucleolin structure and the expression of ribosomal subunit related genes were upregulation, while knockdown of C23 increased the shell-like nucleolin-structure in B-B cloned embryos and downregulated the expression of ribosomal subunit related genes. These results implied that abnormal C23 and ribosome subunit gene expression would lead to the developmental block of iSCNT embryos and ZGA

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Nucleoli in embryos: a central structural platform for embryonic chromatin remodeling?

Cited by 14 publications

References 78 publications

Regulation and Roles of the Nucleolus in Embryonic Stem Cells: From Ribosome Biogenesis to Genome Organization

Regulation and Roles of the Nucleolus in Embryonic Stem Cells: From Ribosome Biogenesis to Genome Organization

Nucleolus and rRNA Gene Chromatin in Early Embryo Development

C23 gene regulates the nucleolin structure and biosynthesis of ribosomes in bovine intraspecific and interspecific somatic cell nuclear transfer embryos

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